The

Veterinary Journal
The Veterinary Journal 166 (2003) 205–209
www.elsevier.com/locate/tvjl

Observations on aggregated lymphoid nodules in the cardiac

glandular areas of the Bactrian camel (Camelus bactrianus)
Wen-Hui Wang *

College of Veterinary Medicine, Gansu Agricultural University, Lanzhou, Gansu 730070, China
Accepted 23 September 2002

Abstract

Aggregated lymphoid nodules are an important part of the gut-associated lymphoid tissue (GALT). They are mainly distributed
in the ileum and appendix of animals and humans but their distribution in the cardiac glandular area has not been reported. A study
of stomach histology in the Bactrian camel has revealed that the nodules are distributed as a band-like region along the ventral wall
of the stomach neck, at the beginning of the cranial enlargement and on the lesser curvature. The mucous folds are thicker in these
regions than where there are no aggregated lymphoid nodules. The nodules appeared similar to ileal aggregated lymphoid nodules
found in other animals and consisted of typical polymorphological lymphatic nodules arranged in a single continuous row occu-
pying the submucosa and forming mucosal folds together with the mucous membrane. The whole mucous membrane with cardiac
glands, diffuse lymphatic tissue and solitary lymphoid nodules in the lamina propria were found to cover the aggregated lymphoid
nodule regions, but some nodules with a typical corona extended into the lamina propria and were covered with follicle-associated
epithelium devoid of cardiac glands. These findings indicate that the stomach of the Bactrian camel possesses not only a special
structure of digestion but also has characteristic immunological morphology.
Ó 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Cardiac glandular area; Aggregated lymphoid nodules; Bactrian camel

1. Introduction bution in the stomach has not been reported (Husband

The alimentary tract has a major immunological role
and a large number of mucosal-associated lymphoid
tissue (MALT) is found in animals and humans. Gut-
associated lymphoid tissue (GALT) plays an essential
role in cellular nutrition, energy metabolism as well as in
immunity. The physio-chemical and immunological
specific properties of the IgA produced by GALTÕs
plasma cells differ from those in serum since it is secreted
into the intestine by gut mucosal epithelium (Dewitt and
Kudsk, 1999; Shields, 2000; Hayday and Viney, 2000).
GALT consists of lymphatic nodules, diffuse lymphatic
tissue, intraepithelial lymphoid cells, follicle-associated
epithelium (FAE) and eosinophils. Lymphatic nodules
may be solitary or aggregated and both types are found
in the tonsil, ileum and appendix although their distri-
*
Tel.: +86-931-7631229; fax: +86-931-766-8010.
E-mail address: wwh777@sohu.com (W.-H. Wang).
and Watson, 1978).
There is little information about GALT in the camel.
Alluwaimi et al. (1998) observed the morphological
features of ileal aggregated lymphoid nodules in the
dromedary camel and found that they differed from
those in sheep and cattle by having a characteristic cup-
shaped structure. We have investigated GALT in the
stomach of the Bactrian camel and report here the
morphological and histological features observed.
2. Materials and methods
Histological samples from different regions of the
cardiac glandular area of the stomach were taken from
20 healthy Bactrian camels aged 3–14 years old from the
Alashan Right Banner of Inner Mongolia, China. The
samples were fixed in 10% formalin, and paraffin sec-
tions were made and stained with haematoxylin and

1090-0233/$ - see front matter Ó 2002 Elsevier Science Ltd. All rights reserved.
doi:10.1016/S1090-0233(02)00263-0
206 W.-H. Wang / The Veterinary Journal 166 (2003) 205–209

eosin as well as Gordon–SweetÕs, van GiesonÕs, Weig-

ertÕs and toluidine blue. The sections were examined
under the microscope for reticular fibre, collagen fibre,
elastic fibre and mast cells. Samples were also fixed in
CarnoyÕs solution and stained with methyl green and
pyronine for plasma cells. Other samples were fixed with
10% calcium formaldehyde and a frozen section made
and stained with seshhexazomium-p-rosaniline a-acetic
ether to show the distribution of T cells.

3. Results

The aggregated lymphoid nodules were located only

in the cardiac glandular area of the third compartment Fig. 2. A portion of mucosal fold: the lymphatic nodules occupying the
of the stomach. This area possesses a special mucosal submucosa are arranged in a row and there are solitary lymphoid
nodules in the lamina propria. Stained with haematoxylin–eosin, 40.
surface in the camel consisting of two regions with re-
ticular and longitudinal mucosal folds. The aggregated
lymphoid nodules formed a long triangle-like region and
were distributed along the ventral walls of the stomach
neck, the beginning of the cranial enlargement and
along the lesser curvature. They started in the reticular
mucosal folds and had a width of 5–7 cm extending into
the boundary area of two regions for about 16–20 cm
ending in the longitudinal mucosal folds with a width of
2 cm with only three or four folds. The mucosal folds in
the aggregated lymphoid nodule area were thicker than
those in the non-aggregated lymphoid nodule region.
The aggregated lymphoid nodule area was greyish-yel-
low, while the non-aggregated lymphoid nodule area
was greyish-white after fixing in 10% formalin. There
was a clear dividing line between the two regions (Fig. 1).
Aggregated lymphoid nodules are formed by the ag-
gregation of simple continuous lymphatic nodules and Fig. 3. The lymphatic nodules are arranged in more rows. Stained with
haematoxylin–eosin, 100.
are concentrated in the submucosa layer in the camel
stomach. They formed mucosal folds together with the
mucous membrane. The nodules were distributed along nodules in young camels were more developed than
the mucosal folds (Fig. 2) although some nodules were those in adult camels and both the number and the size
arranged in two or more rows, especially at the top of of the nodules decreased as the animal matured.
wide mucosal folds (Fig. 3). The aggregated lymphoid The whole of the mucous membrane with the cardiac
glands, diffuse lymphatic tissue and solitary lymphoid
nodules in the lamina propria was covered over the
patches. Some lymphatic nodules with a typical corona
usually extended into the lamina propria, were covered
with FAE and were devoid of glands, and these nodules
were pyramidal or wine-bottle shaped (Figs. 4 and 5).
The aggregated lymphoid nodules had a typical
structure with a distinct germinal centre and were of
different sizes and shapes (round, oval, cuneiform and
irregular shapes). The germinal centre had a pale stain
and consisted mainly of large and middle lymphocytes
and reticular cells, and occasionally macrophages
phagocytosing granules were observed. B cells were
Fig. 1. The clear boundary between the aggregated lymphoid nodule predominant in the germinal centre, and the peripheral
(above) and the non-aggregated lymphoid nodule (below) areas in the area of the nodules had predominant T cells strongly
longitudinal folds. stained and composed of small lymphocytes.
 W.-H. Wang / The Veterinary Journal 166 (2003) 205–209
Fig. 4. The bottom of a mucosal fold: the nodules invading into the
lamina propria have typical corona. Stained with haematoxylin–eosin,
40.
Fig. 5. Bottle-shaped lymphatic nodules. Stained with alcian blue,
100.
There were plenty of endothelial capillaries in the
nodules. Reticular fibres were mainly distributed in the
border area of the nodules with just a few scattered in
the centre (Fig. 6). The corona was made up of compact
small lymphocytes, which were more deeply stained than
those in the germinal centre, and contained a few re-
ticular fibres. A few plasma cells were seen under the
corona.
Some diffuse lymphatic tissue and loose connective
tissues were seen among the follicles. The diffuse lym-
phatic tissue consisted of numerous reticular fibres,
small lymphocytes and a few plasma cells, of which, T
cells predominated. The loose connective tissue sur-
rounding the follicles contained some mast cells, which
were in groups of three to five, or dispersed. They were
of different cell sizes, with many granules in the cyto-
plasm. Endothelial capillaries and venules and collagen
fibres were observed around the follicles (Fig. 7).
The FAE was composed of simple columnar epithe-
lium (with cells demonstrating basophilic plasma and
207
Fig. 6. A portion of a mucosal fold: aggregated lymphoid nodules are
covered with mucous membrane and show reticular fibre distribution.
Gordon–SweetÕs staining, 100.
Fig. 7. Diffuse lymphatic tissue around the nodules showing a rich
supply of endothelial capillaries and venules. Stained with haemat-
oxylin–eosin, 400.
round nuclei), and had been infiltrated by some lym-
phocytes. M cells were oval or cuboid with a round and
deeply stained nucleus located in the centre of the cell.
Scattered lymphatic tissue, mainly composed of small
lymphocytes, plasma cells and macrophages, was found
between the glands of the mucous membrane covered
with aggregated lymphoid nodules, and these cells were
distributed in the mesh of the reticular fibres. Solitary
lymphoid nodules without an evident germinal centre
were also observed between the glands and they were
formed by the aggregation of small lymphocytes. The
muscularis mucosa separated the lamina propria from
the submucosa containing the aggregated lymphoid
nodules, but sometimes was cut off by lymphatic nod-
ules. Solitary lymphatic nodules were observed in the
lamina propria and the submucosa in non-aggregated
lymphoid nodule regions of both the reticular and the
longitudinal mucosa and there were diffuse lymphatic
208 W.-H. Wang / The Veterinary Journal 166 (2003) 205–209
Fig. 8. A boundary between the aggregated lymphoid nodule region
and the non-aggregated lymphoid nodule region. Stained with hae-
matoxylin–eosin, 40.
tissues between the glands. There was a clear boundary
between the aggregated lymphoid nodule region and the
non-aggregated lymphoid nodule region (Fig. 8).
4. Discussion
The Bactrian camel stomach consists of three com-
partments, in which there are two glandular sac areas in
the first compartment and one in the second. The third
compartment, the abomasum, is divided into three
parts: the cardiac glandular area, the fundic glandular
area and the pyloric glandular area. The structure of the
glandular sac area is different from that of other rumi-
nants and much research has been focused on the
anatomy and histology of the stomach as a special di-
gestive organ. The aggregated lymphoid nodules dis-
tributed in the stomach, especially in the cardiac
glandular areas, have not been reported in any of the
studied animals (Wang et al., 2000; Fayed and Makita,
1997; Singh et al., 1996; Dougbag and Berg, 1980;
Hegazi, 1950; Hansen and Schmidt-Nielsen, 1957). The
stomach of the camel possesses a characteristic immu-
nological morphology and is an important immune
organ.
Aggregated lymphoid nodules are an important
composition of GALT and the sites where antigens are
recognized and are transported to the mucosa by M cells
and induce an immune response. Aggregated lymphoid
nodules have a facilitative effect on the healing of in-
testinal wounds by promoting both epithelial cell mi-
gration, epithelial cell proliferation in the crypts
adjacent to the wound and by decreasing the rate of
wound contraction (Saxena et al., 1997). The aggregated
lymphoid nodules are distributed over the tonsil, ileum
and appendix of animals and humans and in the gut
they are concentrated on the wall of the small intestine,
mostly in the ileum.
The mucosal surface on the aggregated lymphoid
nodules is elevated and usually devoid of villi and in-
testinal glands, but with FAE overlying it. The shape,
number, distribution of the aggregated lymphoid nod-
ules and the number, size, shape and arrangement of the
aggregated lymphoid nodules vary with different animal
species, ages, different regions of the alimentary tract
and the diet. For example, in the dromedary camel, the
ileal nodules are distributed mainly in submucosa and
rarely in lamina propria and cup-shaped mucosal ele-
vations; the lymphatic nodules distribute along the lat-
eral borders and at the bottom of the patches, and are
devoid of gut villi. Each patch consists of 25–38 nodules
(Alluwaimi et al., 1998). In sheep and cattle, aggregated
lymphoid nodules are usually in a narrow band; the
nodules are elongated or rod-shaped in sheep and are
oval or elongated in cattle. They are usually arranged in
a row, or two to three rows in young cattle. The mucosa
above the aggregated lymphoid nodules have the intes-
tinal villi and the lymphatic nodules within the ileal
submucosa leading to the elevation of the mucosa into
folds of various orders in sheep or to the elevation of the
ileal mucosa into longitudinal folds in cattle (Alluwaimi
et al., 1998; Roynolds and Morris, 1983; Lalitha, 1991).
In pigs, the ileal aggregated lymphoid nodules are also
present as long-band-like structures (Ma, 1995; Barman
et al., 1997). However in the mouse, the patches are
scattered over all the small intestines and each patch
consists of four to 10 lymphatic nodules. In humans
there are about 30–80 aggregated lymphoid nodules and
each is composed of five to 900 lymphatic nodules
(Chen, 1993).
The mucosa surface of the cardiac glandular area in
the camel consists of reticular mucosal folds and
longitudinal mucosal folds with aggregated lymphoid
nodules in both regions. The mucosa surface over the
patches was clearly different from other animals and
that the mucosa had reticular and longitudinal forms.
However, the aggregated lymphoid nodule region in
the Bactrian camel also had a band-like region similar
to that found in cattle, sheep and pigs, although it
gradually became narrow from the reticular region
to the longitudinal region and looked more like a
triangle.
The histological structure of the aggregated lymphoid
nodules in the stomach of the Bactrian camel was sim-
ilar to that of ileal aggregated lymphoid nodules in the
dromedary and other animals, however, the patches
were aggregated by a single layer of typical polymor-
phological lymphatic nodules. In some areas, the lym-
phatic nodules were arranged in rows as in the ileal
aggregated lymphoid nodules of young cattle.
The aggregated lymphoid nodules in young camels
were more developed than those in adults and both
number and size of the nodules decrease as the animal
matures. Similar changes in ileal aggregated lymphoid
 W.-H. Wang / The Veterinary Journal 166 (2003) 205–209
nodules in the dromedary as well as in sheep and cattle,
have been reported and may be related to the physio-
logical atrophy.
There is no information in the literature about the
existence of the aggregated lymphoid nodules in the
stomach of other animals and the present results indi-
cate that the presence of the aggregated lymphoid nod-
ules in the cardiac glandular area may be specific to the
camel. The fine structure and functions of the aggre-
gated lymphoid nodules need further investigation.
References
Alluwaimi, A.M., Fath El-Bab, M.R., Ahemed, A.K., Ali, A.M.A.,
1998. Studies on the ileal lymphoid tissue (PeyerÕs patches) in
camels, Najdi sheep and cattle. Journal of Camel Practice and
Research 5, 13–18.
Barman, N.N., Bianchi, A.T., Zwart, R.J., Pabst, R., Rothkotter, H.J.,
1997. Jejunal and ileal PeyerÕs patches in pigs differ in their
postnatal development. Anatomy and Embryology 195, 41–50.
Chen, L., 1993. Histology. PeopleÕs Publishing House, Beijing.
Dewitt, R.C., Kudsk, K.A., 1999. The gutÕs role in metabolism,
mucosal barriers function, and gut immunology. Infectious Disease
Clinics of North America 13, 465–481.
Dougbag, A.S.A.M., Berg, R., 1980. Morphological observations on
the normal cardiac glands of the camel (Camelus dromedaries).
Anatomischer Anzeiger 148, 258–264.
209
Fayed, H.M., Makita, 1997. Lectin histochemistry of the glandular
part of the gastric mucosa of the one-humped camel (Camelus
dromedaries). Acta Histochemica et Cytochemica 20, 423–431.
Hansen, A., Schmidt-Nielsen, K., 1957. On the stomach of the camel
with special reference on the structure of its mucous membrane.
Acta Anatomia 31, 353–357.
Hayday, A., Viney, J.L., 2000. The ins and outs of body surface
immunology. Science 290, 97–100.
Hegazi, A.H., 1950. The stomach of the camel. British Veterinary
Journal 106, 209–213.
Husband, A.J., Watson, O.L., 1978. Immunity in the intestine.
Veterinary Bulletin 48, 911–924.
Wang, J.-L., Lan, G., Wang, G.-X., Li, H.-Y., Xie, Z.-M., 2000.
Anatomy subdivisions of the stomach of the Bactrian camel
(Camelus bactrianus). Journal of Morphology 244, 1–7.
Lalitha, P.S., 1991. Gut associated lymphoid tissue in Indian buffalo
(Bubalus bubalis). Indian Veterinary Journal 68, 1057–1059.
Ma, Z., 1995. Anatomy, Histology and Embryology of Domestic
Animals. Agricultural Publishing House, Beijing.
Roynolds, J.D., Morris, B., 1983. The evolution and involution of the
PeyerÕs patches in foetal and postnatal sheep. European Journal of
Immunology 13, 627–635.
Saxena, S.K., Thompson, J.S., Sharp, T.G., 1997. Role of organized
intestinal lymphoid aggregates in intestinal regeneration. Journal of
Investigative Surgery 10, 97–103.
Shields, J.W., 2000. The functional evolution of GALT: a review.
Lymphology 33, 47–57.
Singh, M., Nagpal, S.K., Singh, Y., 1996. Histolomorphological
studies on the glandular mucosa of rumen, reticulum and omasum
in camels (Camelus dromedaries). Indian Journal of Animal
Sciences 66, 881–884.